Sudan Journal of Medical Sciences Volume 16, Issue no. 4, DOI 10.18502/sjms.v16i4.9943 Production and Hosting by Knowledge E Research Article Association Between Smoking and Foot Ulcer among Patients with Diabetes Mellitus, Wad Medani, Sudan Abeer AbdElrahman Elnour Eltilib Department of Family Medicine, Faculty of Medicine, University of Gezira, University City, Wad Medani, Gezira State, Sudan ORCID: Abeer AbdElrahman Elnour Eltilib: https://orcid.org/0000-0002-7093-2757 Abstract Background: This study aimed to assess the relationship between smoking and diabetic foot ulcer (DFU) among adult diabetic patients presenting to Aldarga Diabetic Center, Wad Medani, Sudan in 2020. Methods: This comprehensive study is based on primary data obtained via a longitudinal cross-section random sample of 400 patients with diabetes mellitus who presented to Aldarga Diabetic Health Center in Wad Medani Town, Gezira State, Sudan between September and December 2020. Data were collected using a structured questionnaire. The core questions included two main dimensions: sociodemographic variables and smoking. Data were analyzed using the SPSS software, v.20, using descriptive and inferential statistics, namely, frequency tables and graphs, showing the Chi-square test of the relationship between the dependent and the independent variables. Results: Of the 400 participants, 96 were clearly diagnosed with foot ulcer giving a proportion of 33% in the sample. There was a statistically significant relationship between smoking and DFU. A Chi-square test was done to measure the relationship between smoking and foot ulcer, which was significant at P = 0.043. Conclusion: Extensive awareness programs to control the negative effect of smoking in accelerating DFU and amputation are necessary. Keywords: prevalence of diabetic foot ulcer, diabetic, diabetic food ulceration, smoking 1. Introduction A total of 12,089 diabetic cases were reported in Africa in 2010; this increased to 19,406.8 cases in 2019, which led to the prediction of the number for 2030 and 2045 as 28,629.4 and 47,133.7, respectively. According to the International Diabetes Federation (IDF) Diabetes Atlas, 9𝑡ℎ edition [1]. How to cite this article: Abeer AbdElrahman Elnour Eltilib (2021) “Association Between Smoking and Foot Ulcer among Patients with Diabetes Mellitus, Wad Medani, Sudan,” Sudan Journal of Medical Sciences, vol. 16, Issue no. 4, pages 450–463. DOI 10.18502/sjms.v16i4.9943 Page 450 Corresponding Author: Abeer AbdElrahman Elnour Eltilib; email: Abeert17@yahoo.com Received 02 October 2021 Accepted 10 December 2021 Published 31 December 2021 Production and Hosting by Knowledge E Abeer AbdElrahman Elnour Eltilib. This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited. Editor-in-Chief: Prof. Mohammad A. M. Ibnouf http://www.knowledgee.com mailto:Abeert17@yahoo.com https://creativecommons.org/licenses/by/4.0/ https://creativecommons.org/licenses/by/4.0/ Sudan Journal of Medical Sciences Abeer AbdElrahman Elnour Eltilib Prevention of diabetic foot ulceration is critical in order to reduce the asso- ciated high morbidity and mortality rates, and the danger of amputation. It is essential to identify the “foot at risk,” through careful inspection and physical examination of the foot followed by neuropathy and vascular tests. [2] Dubský et al.’s study showed […] a high recurrence rate of DFU during 3-year follow-up period in patients with a primarily healed ulcer, despite regular follow-up and patient education. We also found that the independent risk factors for ulcer recurrence were plantar location of the ulcer, the presence of underlying osteomyelitis, poor glycemic control and an elevated CRP at the time of diagnosis of the first foot ulcer. Knowing these risk factors may allow clinicians and health care systems to target heightened efforts at prevention of ulceration after healing to selected high-risk patients. [3] Furthermore, Al Busaidi et al. [4] stated that: Diabetes is a chronic and costly disease; however, it can be prevented. The alarm of the rising tide of diabetes has not yet been successfully translated into action in the Middle East. The governments in the region need to devise more intense, broader policies and preventive measure programs based on local sociocultural practices to effectively combat the situation. Further improvements of the primary health care system and cross-governmental approaches are needed in the region to keep the growing epidemic of diabetes under control. 1.1. Characteristics, prevalence, and outcomes of diabetic foot ulcers (DFUs) in Africa Rigato and colleagues in a systemic review and meta-analysis reported as follows: Fifty-five full-text papers and ten abstracts were retrieved, reporting data from 19 African countries on 56,173 diabetic patients. According to the data collected, the overall prevalence of foot ulcers was 13% and increased over time, especially since 2001. Approximately 15% of patients with foot lesions underwent major amputation and 14.2% died during hospitalization. In patients with diabetic ulcers, insulin therapy was uncommon and neu- ropathy was the most common predisposing factor, but the prevalence of DOI 10.18502/sjms.v16i4.9943 Page 451 Sudan Journal of Medical Sciences Abeer AbdElrahman Elnour Eltilib peripheral arterial disease correlated with amputation rates. Amputation and mortality decreased over time, probably as result of the implementation of screening programs in the last ten years. Mortality was directly related to previous amputation. [5] Moreover, Elmadhoun and coworkers reported a high prevalence of diabetes mellitus (DM) and glucose intolerance in the urban population of the River Nile State (RNS) [6]. Another study conducted in the same region showed that the prevalence of DFU was 18.1% and that the risk of development of DFU is increased with the increase in the duration of diabetes, especially in those with DM for more than 10 years [7]. Additionally, another study [8] reported a strong relationship between smoking and foot ulcer, the results of the paper stated: The role of smoking for wound healing in patients with diabetic foot has been unclear. This meta-analysis examined the relationship between cigarette smoking and diabetic foot wound healing. Observational studies for the association between smoking and diabetic foot wound healing of patients were systematically searched through PubMed and Wanfang Data, pub- lished up to June 2018. Healing rates of wounds were recognized as out- comes. Meta-analysis models were chosen by heterogeneity. A total of 3388 eligible studies were identified, of which 18 met all our inclusion criteria. In the smoking group, healing rate had an average of 62.1%, ranging from 20.0% to 89.6%; in the nonsmoking group, healing rate had an average of 71.5%, ranging from 40.2% to 93.8%. A significant association was found between smoking and the healing of diabetic foot. Our meta-analysis indicated that smoking had an overall negative effect on the wound healing of diabetic foot individuals. This study provides evidence for the harm of smoking to diabetic foot and may help reduce the medical and economic burden on poor healing of diabetic foot. Furthermore, Taha and Ball’s [9] study on smoking in Africa showed that: Cigarettes are heavily promoted in Africa. Smoking-related diseases have already made their appearance in Africa. The 2 most common types of cancer in the Natal Bantu are lung and esophageal tumors. Lung cancer in Natal men has increased 6-fold and in women about 5-fold over the past 11 years. As a result, tobacco companies have started to diversify and intensify promotion of cigarettes and the growth of tobacco in the 3rd world. DOI 10.18502/sjms.v16i4.9943 Page 452 Sudan Journal of Medical Sciences Abeer AbdElrahman Elnour Eltilib DFU is one of the commonest complications of DM imputed to a number of morbidity and mortality cases in diabetic patients. Nowadays, the incidence of DFU is increasing due to the increased prevalence of diabetes. However, the risk factors of the problem are less or not studied in Gezira State, Sudan. Hence, this study was conducted to assess the determinants of DFU in relation to smoking among adult patients with diabetes attending Aldarga Diabetic Center, Wad Medani, Sudan in 2020. 2. Materials and Methods A longitudinal, cross-sectional design was used to conduct the study among patients presenting at Aldarga Diabetic Health Center in Wad Medani Town, Gezira State, Sudan between September and December 2020. The center is located in the north of Wad Medani town, 186 km south of Khartoum, the capital of Sudan. It was opened as a specialized center for the central region of Sudan. Of the 400 participants who presented at the center, 96 had foot ulcer. 2.1. Sample size and sampling design A random sampling method was used to select the sample of the study (total diabetic patients in 2020 reporting to the diabetic follow-up clinic). The simple random sampling equation for provisional sample size n* was calculated using the following formula: n = (t² × p × q) / (d²), where: n* = required sampling size; p = anticipated population proportion taken as 50% because it gives the maximum possible sample size. If we take the estimated prevalence rate of 0.15 for Sudan as p, the sample size will be 195, however, we preferred a larger sample; t = confidence level, taken as 95%; and d = absolute precision required on either side of anticipated proportion taken as 5%. Next, the provisional sample was multiplied by a design effect of 2 to give the final sample n: n = (2² × 50 × 50) / (25) = 400. A total of 400 participants were successfully compassed by field data collection team. The total diabetic patients who reported to the center in 2020 were 40,507 classified by months with an average of 3376 diabetic patients per month. The procedure used for selecting sampling units was twofold. First, we calculated the systematic sampling interval factor by dividing the number of diabetic patients during DOI 10.18502/sjms.v16i4.9943 Page 453 Sudan Journal of Medical Sciences Abeer AbdElrahman Elnour Eltilib the data collection period (November–December 2020) by the sample size, that is, N/n = 1823/400 = 4.55 ≅ 5. The sample unit number 5 was selected first. The rest of the sampling units were selected according to Kish selection procedure to cater for gender [10]. 2.2. Data analysis Descriptive statistics was initially undertaken to analyze the composition of the sample. Data were coded and entered into a computer using two of the latest versions of prepared packages of statistical analysis namely Statistical Package for Social Sciences (SPSS) v.24.0/25.0 for Windows. The programs were used in different stages of data processing to process the raw data obtained from the questionnaires. Quantitative analysis of the question responses obtained from the questionnaire were summarized, portrayed, and analyzed on a statistical basis in order to offer the researcher the opportunity to analyze the responses and identify whether the results are skewed [10]. The following statistical analyses were run: 1. A pilot study was conducted to establish content validity. 2. Face validity was established through the circulation of the questionnaire to 60 pilot respondents. 3. The summary results of the descriptive statistics were presented using tables and graphs. 2.3. Operational definitions 2.3.1. Diabetic foot The International Working Group on Diabetic Foot (IWGDF) has defined the diabetic foot as infection, ulceration, or destruction of tissues of the foot of a person with currently or previously diagnosed DM, usually accompanied by neuropathy and/or peripheral arterial disease (PAD) in the lower extremity. 2.3.2. Diabetic foot ulcer (DFU) DFUs are nondramatic lesions of the skin on the foot distal to malleoli of a person who has DM [11]. DOI 10.18502/sjms.v16i4.9943 Page 454 Sudan Journal of Medical Sciences Abeer AbdElrahman Elnour Eltilib 2.3.3. Diagnostic criteria for DM or measurement of DM (i) Random plasma glucose value of ≥200 mg/dL (≥11.1 mmol/L) or (ii) fasting plasma glucose value of ≥126 mg/dL (≥7.0 mmol/L) or (iii) a 2-hr oral glucose tolerance test (GTT) value in venous plasma ≥200 mg/dL (≥11.1 mmol/L), or (iv) glycated hemoglobin (HbA1c) ≥6.5% (≥48 mmol/molHb) [12]. 2.3.4. Smoking The act of inhaling and exhaling the fumes of burning plant material. A variety of plant materials are smoked, including marijuana and hashish, but the act is most commonly associated with tobacco smoked in a cigarette, cigar, or pipe. Tobacco contains nicotine, an alkaloid that is addictive and can have both stimulating and tranquilizing psychoactive effects. [13] (i) Respondents’ socioeconomic characteristics The survey data were initially analyzed using frequency tables and descriptive statis- tics. Of the 400 sampled respondents, 55% were male and 44.5% were females living in predominantly extended (68%) families with the majority living in towns (56.8%). While only 8.5% reported high income level, 33.5% reported low income, and the majority were of medium income level (58%). Table 1 shows the frequency distribution and descriptive statistics of the participant’s socioeconomic characteristics. The youngest patient in the sample was 30 years of age and the oldest was 89. The age distribution classified in five years age group shows an expected pattern with sharp skewness to the right, where the majority are over the age of 50 years (79%) and more than half are >60 years of age. The mean age is 59.9 years with approximately similar median and mode indicating that the distribution is mesokurtic showing a confidence interval of 59.9 ± 1.31. The majority of respondents were married (69.3%), 6.8% were single with abnormally nontypical high proportion of widows and divorcees (24%). The majority were either uneducated or had basic education (67.6), 20.3% had secondary education, and only 12.3% had a university degree. These tally very well with occupational classification, as 65.8% were either unemployed (38%), housewives (13.5%), or had unspecified jobs (14.3%). The general picture that can be drawn from the respondents’ socioeconomic status is that diabetic patients reporting to Aldarga Center are mostly of low social class category. (ii) Factors related to respondents’ behavior DOI 10.18502/sjms.v16i4.9943 Page 455 Sudan Journal of Medical Sciences Abeer AbdElrahman Elnour Eltilib Table 1: Frequency distribution and descriptive statistics of major respondent’s indicators. Variable N Percentage (%) Central tendency Standard error of the mean Age (yr) 30–34 15 3.8 35–39 10 2.5 40–44 31 7.8 Mean = 59.5 1.31 45–49 28 7 Median = 60 50–54 42 10.5 Mode = 58 55–59 61 15.3 Skewness = – 0.222 –0.012 60–64 48 12 65–69 57 14.3 Kurtosis = 0.555 0.243 ≥70 108 26.8 Total 400 100 Marital status Single 27 6.8 Median = 2.0 Married 277 69.3 Skewness = 0.976 0.122 Widow 72 18 Mode = 2.0 Divorced 24 6 Kurtosis = 0.132 0.233 Total 400 100 Educational level Illiterate 34 8.5 Khalwa 77 19.3 Median = 3.0 Basic 159 39.8 Skewness = 0.163 0.057 Secondary 81 20.3 Mode = 3.0 University 42 10.5 Kurtosis = 0.232 0.223 Postgraduate 7 1.8 Total 400 100 Occupation Professional 4 1 Business 60 15 Median = 8.0 Employee and uniform 38 9.6 Skewness = 0.163 0.234 Worker and farmer 35 8.8 Mode = 9.0 Housewife 54 13.5 Kurtosis = 0.232 0.122 Unemployed and others 209 52.3 Total 400 100 Source: Researchers’ own survey, 2020. DOI 10.18502/sjms.v16i4.9943 Page 456 Sudan Journal of Medical Sciences Abeer AbdElrahman Elnour Eltilib Figure 1: Relationship between smoking and diabetic foot ulcer. Figure 2: Relationship of diabetic foot ulcer with smoking frequency per day. The majority of the respondents were nonsmokers and also nonalcoholic drinkers – 40.0% and 50.5%, respectively, and only 9.5% were snuffers. In addition, only 12% were smokers and about 4.3% of them smoked more than once daily (7.8%). A Chi-square test was done to measure the relationship between smoking and foot ulcer, which was significant at P-value = 0.043. DOI 10.18502/sjms.v16i4.9943 Page 457 Sudan Journal of Medical Sciences Abeer AbdElrahman Elnour Eltilib Figure 3: Relationship of diabetic foot ulcer with drinking of alcohol. Figure 4: Relationship of diabetic foot ulcer with the use of snuff. 3. Results 3.1. Respondent’s socioeconomic characteristics and association with smoking The survey data were initially analyzed using frequency tables and descriptive statistics. Of the 400 sampled respondents, 55.5% were males and 44.5% were females living DOI 10.18502/sjms.v16i4.9943 Page 458 Sudan Journal of Medical Sciences Abeer AbdElrahman Elnour Eltilib Table 2: Chi-square test of the relationship between the dependent (foot ulcer) and independent variables (smoking). Decision DF X2 SIG Decision Smoking 1 4.08 0.043 Frequency of smoking per day 2 4.09 0.129 Alcohol intake 1 0.263 0.608 Use of snuff 1 0.717 0.397 Source: Researchers’ own data. in predominantly extended (58%) families with the majority living in towns (56%). Only 8.5% reported high income level, 33.5% reported low income, and the majority were of medium income level (58%). Table 3 shows the frequency distribution and descriptive statistics of the participant’s socioeconomic characteristics. The youngest patient in the sample was 30 years old and the oldest was 89. The age distribution classified in five years age group shows an expected pattern with sharp skewness to the right, where the majority were >50 years (79%) and more than half >60 years of age. The mean age was 59.9 years with approximately similar median and mode indicating that the distribution is mesokurtic showing a confidence interval of 59.9 ± 1.31. The majority of respondents were married (69.3%), 6.8% were single with abnormally nontypical high proportion of widows and divorcees (24%). The majority were either uneducated or had basic education (67.6), 20.3% had secondary education, and 12.3% were in the category of university and over. These tally very well with occupational classification as 65.8% were either unemployed (38%), housewives (13.5%), or had unspecified jobs (14.3%). The general picture that can be drawn from the respondent’s socioeconomic status is that diabetic patients reporting to Aldarga center are of low social class category. Additionally, 20% of the respondents smoked, which was significant at p-value = 0.043, where the drinking of alcohol was only 3% and snuffer was 17%. 4. Discussion This study, to the best of our knowledge, could be the first to estimate the association between smoking and DFU in Gezira state, Sudan. Of the 400 DM participants included in this study, 96 had DFU, of which 12% were smokers, P-value = 0. .043The finding of this study is in line with the study of Xia et al. [14], who stated that: DOI 10.18502/sjms.v16i4.9943 Page 459 Sudan Journal of Medical Sciences Abeer AbdElrahman Elnour Eltilib Table 3: Frequency distribution and descriptive statistics of the participant’s socioeconomic characteristics. Total % �2 P-value Age of the respondents (yr) 30–39 25 6.2 20.81 0.035 40–49 59 14.8 50–59 103 25.8 60–69 105 26.2 70–79 90 22.5 80–89 18 4.5 Sex of the respondents Male 222 55.5 1.682 0.116 Female 178 44.5 Residence of the respondents Town 225 56 0 0.54 Village 175 44 Type of family Nuclear 168 42 0.353 0.229 Extended 232 58 Income level Low 134 33.5 0.736 0.612 Medium 232 58 High 34 8.5 Marital status Single 27 6.8 0.451 0.93 Married 277 69.2 Widow 72 18 Divorced 24 6 Diabetic in the family Yes 194 49 2.033 0.09 No 206 51 Type of work of the respondent Professional/Business64 16 13.32 0.1 Employee 35 8.8 Worker 15 3.7 Farmer 20 5 Uniform 3 0.8 Housewife 54 13.5 Other 57 14.2 Unemployed 152 38 Educational level Illiterate 34 8.5 7.496 0.186 Khalwa/Madrasa 77 19.3 Basic 159 39.8 Secondary 81 20.2 University/Postgraduate49 12.2 Smoking Yes 77 20 4.08 0.043 No 323 80 Frequency of smoking per day More than once in the day 50 13 4.09 0.129 Daily 27 7 No application 323 80 Drinking of alcohol Yes 10 3 0.263 0.608 No 390 97 Use of snuff Yes 67 17 0.717 0.397 No 333 83 Total 400 DOI 10.18502/sjms.v16i4.9943 Page 460 Sudan Journal of Medical Sciences Abeer AbdElrahman Elnour Eltilib At the end of this review, the current mainstream therapies for smoking cessation are also outlined. We believe that it is urgent for all diabetic patients to quit smoking so as to reduce their chances of developing foot ulcers and to improve the prognosis of diabetic foot ulcers. On the other hand, Pal and colleagues [15] showed that: The diabetic patients who were smokers and/or chronic alcoholic underwent more amputations with concomitant longer hospital stay than the patients who had no addiction to these substances. The prognosis was worse in the subgroup of patients who were both smoker and chronic alcoholic. The study was done on 89 patients who were admitted in the surgical wards of the following teaching hospitals in India - KPC Medical College and Hospital as in our study those they had foot ulcer compared in those not had DFU were more smokers, snuffers and alcoholic’s [12%, 7.3%,9.5%, 7.3%,1.5%, 1%] and as we know from medicine their effect on dealing wound healing and accelerating DFU. Moreover, public databases, including PubMed and Embase, were searched for articles published prior to February 29, 2016. Heterogeneity was assessed using the Cochran’s Q statistic and the I2 statistic, and odds ratio (OR) and 95% confidence interval (CI) were calculated and pooled appropriately. Sensitivity analysis was performed to evaluate the stability of the results of the present meta-analysis which suggested that smoking is a notable risk factor for diabetic foot amputation. Liu et al. reported that smoking cessation appears to reduce the risk of diabetic foot amputation [15]. All studies showed a strong association between increased smoking and DFU. The effects of cigarette smoking on DFUs are clear from our study and other papers. Our study found that smoking had a negative effect in wound healing in foot ulcer cases. Hence, if the factors associated with DFU reduces such as quitting smoking, majority of our patients can be saved from DFU and disabilities arising thereof. Acknowledgements The authors express their sincere appreciation to Wad Medani ALderaga Health Center in Gezira State, Sudan for their cooperation. They are also thankful to the diabetic patients who willingly participated in the research. DOI 10.18502/sjms.v16i4.9943 Page 461 Sudan Journal of Medical Sciences Abeer AbdElrahman Elnour Eltilib Ethical Considerations Before initiating the field survey, the objective of ethics in research was ensured by obtaining ethical clearance from the Director of Health Affairs in Wad Medani locality of Gezira State. A supportive formal letter was written to Aldarga Diabetic Center. Data collection was done after permissions were obtained from the center managers, and oral informed consent was obtained from the study participants to start data collection after assuring them of the ethical aspects regarding the confidentiality, privacy, and consent of the data. Competing Interests None declared. Availability of Data and Material All relevant data and methodological details pertaining to this study are available to any interested researchers upon reasonable request to corresponding author. Funding This research received no specific grant from any funding agency in the public, com- mercial, or not-for-profit sectors. References [1] International Diabetes Federation (IDF). (2019). IDF Diabetes Atlas (9𝑡ℎ ed.). IDF. [2] Alexiadou, K. and Doupis, J. (2012). Management of diabetic foot ulcers. Diabetes Therapy, vol. 3, article 4. [3] Dubský, M., Jirkovská, A., Bem, R., et al. (2013). Risk factors for recurrence of diabetic foot ulcers: prospective follow-up analysis in the Eurodiale subgroup. International Wound Journal, vol. 10, no. 5, pp. 555–561. [4] Al Busaidi, N., Shanmugam, P., and Manoharan, D. (2019). Diabetes in the Middle East: government health care policies and strategies that address the growing diabetes prevalence in the Middle East. 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A study on the impact of smoking and alcoholism as determinant factors in the prognosis and outcome of diabetic foot ulcer disease. International Journal of Research in Medical Sciences, vol. 4, no. 5, pp. 1720–1724. [15] Liu, M., Zhang, W., Yan, Z., et al. (2018). Smoking increases the risk of diabetic foot amputation: a meta-analysis. Experimental and Therapeutic Medicine, vol. 15, pp. 1680–1685. DOI 10.18502/sjms.v16i4.9943 Page 463 Introduction Characteristics, prevalence, and outcomes of diabetic footulcers (DFUs) in Africa Materials and Methods Sample size and sampling design Data analysis Operational definitions Diabetic foot Diabetic foot ulcer (DFU) Diagnostic criteria for DM or measurement of DM Smoking Results Respondent's socioeconomic characteristics and association with smoking Discussion Acknowledgements Ethical Considerations Competing Interests Availability of Data and Material Funding References